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Surviving overwinter in northern areas is challenging for vertebrate herbivores (Boonstra 2004). Winter combines the challenges of cold temperatures, snow, food scarcity and, often, high predation. Winter thus provides a template against which strong natural selection may occur, with only those individuals best able to obtain and to allocate resources surviving to the subsequent breeding season.
Strategies for surviving winter vary with an organism's body size and physiological flexibility. For mammals that weigh < 1 kg, strategies include food caching (e.g. red squirrels, Tamiasciuris hudsonicus, pikas, Ochotona princeps), alteration of fur to obtain greater insulation (Chappell 1980; Steudel, Porter & Sher 1994), and use of microclimate refugia such as subnivean spaces and dens, which are warmer than the ambient temperatures (e.g. lemmings, pikas, weasels) (Chappell 1980). Body-mass changes, with concomitant changes in energetic requirements, are also common. In ground-dwelling sciurids that hibernate, intense hyperphagy to increase body mass is essential for survival. For animals that stay active throughout winter, such as shrews and microtine rodents, reducing body mass to reduce energy requirements and foraging time is a common strategy termed Dehnel's phenomenon (Brown 1973; Iverson & Turner 1974; Heldmaier & Steinlechner 1981; Hansson 1990). For some small mammals, reductions in body mass are linked to photoperiod; they occur even when temperatures are maintained and animals are allowed ad libitum food [e.g. hamsters Phodopus sungorus, Heldmaier & Steinlechner (1981); meadow voles Microtus pennsylvanicus, Dark & Zucker (1986)].
For medium-sized mammals, such as snowshoe hares (Lepus americanus, Erxleben, ∼1·5 kg), it is not clear whether the mass loss is the adaptive Dehnel's phenomenon or a consequence of environmental conditions. The body-mass dynamics of hares are fundamentally different from those of voles (Aars & Ims 2002): juvenile hares do not stop growing before winter, and when mass loss occurs it is gradual and occurs throughout the winter. Presumably these differences between hares and voles are related to fat storage and metabolism. Snowshoe hares do not undertake hyperphagy, and their fat stores provide only a few days of support prior to starvation (Whittaker & Thomas 1983), so mass loss is likely to involve more than fat stores. Some researchers suggest that mass loss derives from direct food limitation, especially when hare populations are at cyclic peaks or declining (Keith & Windberg 1978; Vaughan & Keith 1981). This pattern would be akin to the mass dynamics of ungulates, which commonly experience food stress overwinter (DelGiudice, Peterson & Samuel 1997; DelGiudice et al. 2000) but also undergo seasonal mass fluctuations in the presence of superabundant food (Cowan, Wood & Kitts 1957). Alternatively, predation risk may affect foraging behaviour (Hik 1995; but see Hodges 1999; Hodges & Sinclair 2003) and stress physiology (Boonstra et al. 1998), and either of these responses could cause mass loss even in the presence of an adequate food supply. Overwinter mass loss in snowshoe hares is not affected by reproduction, because weaning occurs by the end of September and pregnancies are initiated typically in April in our Yukon study area.
In this paper, we use data from a snowshoe hare cycle in south-western Yukon (see Krebs, Boutin & Boonstra 2001a for a full description of this long-term study and its results), with experimental treatments of fertilization, food-supplementation, terrestrial predator-exclosure and food-supplementation plus predator-exclosure to test the following hypotheses about snowshoe hare mass loss overwinter. (1) Mass loss is an adaptive overwinter strategy to minimize energy needs, irrespective of food supply. In this case, snowshoe hares on all treatments should lose mass overwinter. The amount might be correlated with winter severity. (2) Mass loss results from food limitation. If so, then mass loss should be more prevalent during peak and decline years. Snowshoe hares on fertilized or food-supplemented areas are more likely to maintain mass. Body-fat stores should reflect food availability. (3) Mass loss results from behavioural and physiological responses to predation risk. Mass loss should be most pronounced during periods of highest predation. Hares inside the predator-exclosures should maintain their mass. Body fat should be reduced in animals exposed to higher predation risk. (4) Mass loss is an artefact of measuring mass loss based on populations (mean spring mass − mean autumn mass), which could be affected by differential survival of animals overwinter. Some previous studies have used this metric rather than an analysis of individuals caught both in autumn and in spring.
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- Methods and materials
Snowshoe hares clearly had the capacity to maintain or gain mass overwinter in all years of the population cycle. However, the proportion of animals doing so and the amount of mass change varied substantially. This variation in mass-change patterns was affected by a complex interplay of food availability, risk of predation, autumn body mass and snow conditions. These patterns suggest that body mass is a plastic trait that responds as animals balance conflicting demands. Our results do not support the common argument that overwinter mass loss by snowshoe hares is driven primarily by absolute food shortage (Newson & de Vos 1964; Keith & Windberg 1978; Vaughan & Keith 1981; Keith et al. 1984). Instead, some hares lost mass even when food was superabundant, some hares gained mass even in severe winters and other factors also influenced overwinter mass dynamics (Table 1).
Table 1. Synopsis of overwinter mass loss hypotheses, predictions and results for snowshoe hares
|A priori hypotheses|
|(1) Mass loss is an adaptive overwinter strategy to minimize energy needs||Hares on all treatments should exhibit overwinter mass loss||Possibly supported but too simplistic. Some hares on all treatments lost mass, but others gained mass. Mass dynamics were also affected by food supply, predation risk and autumn mass|
|(2) Mass loss results from food limitation||Hares should lose more mass during peak and decline years||Accept hypothesis with reservations. Mass loss on control areas was most severe during the decline phase but food limitation interacted with predation pressure|
|(3) Mass loss results from behavioural and physiological responses to predator pressure||Mass loss should be most pronounced during periods of highest mortality and should not occur in predator reduction sites||Accept hypothesis. Predator-exclosures reduced or stopped overwinter mass loss, which was completely eliminated in the predator-exclosure + food treatment|
|(4) Mass loss is an artefact of measuring mass loss based on populations rather than individuals||Mass loss overwinter will not be found if individuals are followed overwinter||Reject hypothesis. Overwinter mass loss does occur but is poorly predicted by population mean measurements|
|(5) Autumn mass affects overwinter mass dynamics|| ||Small hares gained mass and heavy hares lost mass overwinter, irrespective of food supply and predation risk|
|(6) Snow depths affect mass loss|| ||Hares lost more mass in winters with deeper snow|
Snow depths appeared to impose energetic costs on hares, with deeper snow correlated with more mass loss. The decline winters had deeper snows than most other winters during this cycle, thus partly confounding cyclic phase and snow depth. However, our primary goal was to explore how the experimental manipulation of food and predators affected hares, and the treatments had clear impacts on mass change within years: when costs of obtaining food declined via either mechanism, snowshoe hares were more likely to maintain or gain mass. Snowshoe hare density had no impact on mass change patterns, indicating that hares were not directly competing for resources. The impacts of food supply and predation risk interacted with autumn mass, because across all treatments light animals were likely to gain mass, and heavy animals to lose it. Although we have insufficient sample sizes to tell conclusively if small animals grew to larger final body sizes on the food addition or predator-exclosure + food treatments, we suspect that this is likely.
Predation risk also influenced overwinter mass dynamics. Low overwinter survival rates corresponded to the most severe mass loss, and virtually all hares that disappeared did so because they were killed by predators, with 80–100% of the deaths of radio-collared hares caused by predators (Krebs et al. 1995; Hodges et al. 1999). Survival was extremely low during the decline (survival on the control grids was 0·7%/ year, similar on the two food addition sites (3·7%) and much higher in the predator-exclosures (predator-exclosure 9·5%; predator-exclosure + food 20·8%) (Krebs et al. 1995; Hodges et al. 1999, 2001). Mass loss is affected by high predation risk because of the physiology of the stress response: under conditions of high stress, gluconeogenesis is accelerated, mobilizing body resources and tissues for the formation of glycogen (Boonstra et al. 1998). Glycogen can be converted rapidly to glucose to fuel muscles when a predator threatens survival.
Our results also show clearly that population-based analyses of mass change are quite different from individual-based estimates. Annually, snowshoe hare densities are lowest in the spring and highest in the autumn, so sample sizes of hares often differ substantially between these trapping periods (Hodges et al. 2001), and small spring sample sizes weaken inferential power and could lead to biases. Additionally, population-based estimates are likely to be affected by sampling different numbers of each cohort in the two seasons. For example, females typically weigh more than males, and if different proportions of males and females were caught in the two seasons, that would affect the estimate of mass change. Similarly, if the autumn trapping session contained a different proportion of young-of-the-year than the spring session, that could lead to faulty conclusions about mass dynamics. Such biases could arise either via biological mechanisms such as differential dispersal or mortality of one sex or age class, or via sampling problems such as different trappabilities.
The energetic costs for snowshoe hares overwinter include thermoregulation, foraging effort, warming and digesting food, and mitigating predation risk through habitat selection and movements away from predators (avoiding areas with predator sign, or being chased by predators). Some energetic costs for snowshoe hares are reduced by changes in morphology of hair (Russell & Tumlison 1996), digestive structure (Smith, Hubbart & Shoemaker 1980) and physiology (Irving et al. 1957; Hart, Pohl & Tener 1965; Feist & Rosenmann 1975). Several small mammal species show similar seasonal variation in organ size, lean mass and fat mass (Batzli & Esseks 1992; Virgl & Messier 1992; Piersma & Lindström 1997; Zuercher, Roby & Rexstad 1999; Derting & Hornung 2003). These alterations in proportional mass of different body components facilitate effective digestion of less nutritious foods, minimize the energy expenditures on reproductive organs during nonreproductive times and store energy in different tissue types.
Despite these energy-saving changes, body mass by itself also affects energetic costs. Heavier animals have increased total locomotion costs, especially in deep snow (Buskirk, Ruggiero & Krebs 2001), and higher absolute metabolic rates, thus requiring more food and more foraging time to maintain their mass. Carrying more mass may also impose costs when snowshoe hares try to escape from predators, as has been documented for small birds (Witter & Cuthill 1993; Gosler, Greenwood & Perrins 1995). However, heavier animals also benefit from reduced surface area to volume ratios, which helps to retain heat.
Maintaining an ‘optimal mass’ is therefore a challenging problem for an overwintering snowshoe hare, both because so many variables contribute to what may be optimal and because substantial mass change by hares is a slow process that cannot respond to small environmental fluctuations. Although small birds can adjust their fat stores on a daily basis by adjusting food intake (Gosler 2002), snowshoe hare fat-store changes respond slowly, in large part because their food is low quality (Hodges & Sinclair 2003). Nor is it clear to what extent body mass and composition changes are adaptive or simply responsive to environmental conditions and behavioural decisions. Body mass or changes in condition have been linked to survival or cause of death (Rohner & Krebs 1996; Murray 2002), which suggests overwinter body-mass dynamics are subject to selection.
Fat stores in bone marrow and around kidneys were related weakly to body mass of snowshoe hares. Kidney fat fluctuates seasonally in L. europaeus (European hares, Pepin 1987), and seasonal variation in tissue allocation may prevent a strong relationship between these fat stores and body mass. Marrow fat was associated with the causes of mortality: snowshoe hares that died of non-predation causes had much lower marrow fat than animals killed by predators or humans. Both kidney and marrow fat were higher for animals on the food-supplemented grids, even during winters when the majority of animals on these sites lost mass. These patterns suggest that body mass and internal allocation of energy into different tissues both influence survival overwinter.
Dehnel's phenomenon of overwinter mass loss is at odds with Bergmann's rule of increasing body mass with latitude and winter severity (Ashton, Tracy & de Queiroz 2000; Freckleton, Harvey & Pagel 2003). Explanations for Bergmann's rule have emphasized the thermal advantages of larger bodies: the heat-conservation hypothesis suggests that larger organisms retain heat more efficiently because they have lower surface area to volume ratios (Steudel et al. 1994), while the fasting-endurance hypothesis argues that larger-bodied organisms can maintain larger fat stores, thus tolerating cold and food shortage better (Millar & Hickling 1990). Clearly, if overwinter mass loss is an adaptive strategy for surviving winter, then these two patterns need to be reconciled. Although Bergmann's rule has typically been considered from the standpoint of winter energetics, it is possible that summer or reproductive energetics drive the observed cline in body mass (Speakman 1996). Alternatively, different body masses may be ideal at different times of year, leading to seasonal trade-offs (Michener & Locklear 1990; Smith & Charnov 2001).
We suspect that the complex mass dynamics in snowshoe hares are typical of species that are active overwinter, rather than hibernating or migrating. In addition to the small rodents that were initially described by Dehnel's phenomenon, species such as beavers (Castor canadensis), muskrats (Ondatra zibethica) and porcupines (Erithizon dorsatum) also show complicated patterns of mass loss overwinter, with autumn mass and food supply or foraging costs co-implicated in shaping mass dynamics and juveniles frequently not showing the same patterns as adults (Virgl & Messier 1992; Sweitzer & Berger 1993; Smith & Jenkins 1997). Furthermore, body mass is highly variable multi-annually in cyclic species (voles, Boonstra & Krebs 1979; Norrdahl & Korpimäki 2002; Ergon et al. 2004; snowshoe hares, Keith & Windberg 1978), which suggests further that body mass is variable and is shaped by the costs and benefits of obtaining and expending resources.
Our results do not support the idea that hares lose mass overwinter as a direct reflection of limited food supply. Nor do our data support the idea that overwinter mass loss is an adaptive strategy that reduces energetic expenditures and boosts survival as suggested by Dehnel's phenomenon. Both are refuted because there is substantial variation in individual mass dynamics overwinter and multiple factors beyond food supply influence mass dynamics. We suspect that overwinter mass dynamics are subject to selection, because body-fat stores and foraging behaviour are linked to the risk of predation, but for some hares the optimal strategy probably involves mass gain rather than mass loss. Clearly, winter is a challenging time that requires hares to make the best of a bad situation, with many environmental factors affecting the changes that occur (Table 1). Foraging costs are affected by snow depths, food availability and predation risk, and these factors influenced body-mass dynamics of snowshoe hares overwinter. Starting body mass also has a large influence: very small hares gained mass and very large hares lost mass no matter what the environmental conditions were. Small hares are challenged by this growth overwinter, because their marrow fat is quite low. In contrast, the heaviest hares were able to lose mass while retaining high marrow fat. The costs and consequences of mass change therefore are quite different for these two groups. As with many ecological problems, the challenge is to quantify the relative impact of these different factors and to determine the consequences particular patterns of mass maintenance or change have on subsequent fitness.